SUMMARY

Mantis shrimp are renowned for their unusual method of breaking shells with
brief, powerful strikes of their raptorial appendages. Due to the extreme
speeds of these strikes underwater, cavitation occurs between their appendages
and hard-shelled prey. Here we examine the magnitude and relative contribution
of the impact and cavitation forces generated by the peacock mantis shrimp
Odontodactylus scyllarus. We present the surprising finding that each
strike generates two brief, high-amplitude force peaks, typically
390–480 μs apart. Based on high-speed imaging, force measurements and
acoustic analyses, it is evident that the first force peak is caused by the
limb's impact and the second force peak is due to the collapse of cavitation
bubbles. Peak limb impact forces range from 400 to 1501 N and peak cavitation
forces reach 504 N. Despite their small size, O. scyllarus can
generate impact forces thousands of times their body weight. Furthermore, on
average, cavitation peak forces are 50% of the limb's impact force, although
cavitation forces may exceed the limb impact forces by up to 280%. The rapid
succession of high peak forces used by mantis shrimp suggests that mantis
shrimp use a potent combination of cavitation forces and extraordinarily high
impact forces to fracture shells. The stomatopod's hammer is fundamentally
different from typical shell-crushing mechanisms such as fish jaws and lobster
claws, and may have played an important and as yet unexamined role in the
evolution of shell form.

Mantis shrimp (Crustacea, Stomatopoda) use their greatly enlarged second
thoracic raptorial appendages to smash or spear prey, construct and excavate
burrows, defend against predators and fight with conspecifics
(Caldwell, 1975). In `spearer'
stomatopods, the dactyl is a sharp, spiny, barbed spear, which stabs into
soft-bodied, evasive prey. `Smasher' stomatopods can stab with the sharp tip
of their dactyl or smash with the bulbous heel of the dactyl
(Fig. 1). In order to generate
extreme accelerations with their raptorial appendages, all mantis shrimp
species are thought to utilize a power amplification mechanism consisting of
elastic springs, latches and lever arms
(Burrows, 1969;
Burrows and Hoyle, 1972;
McNeill et al., 1972;
Patek et al., 2004). The click
mechanism holds the limb in place during muscle contraction
(Burrows, 1969;
Burrows and Hoyle, 1972;
McNeill et al., 1972), and a
specialized spring stores and releases elastic energy
(Patek et al., 2004). The
subject of the present study, the `smasher' peacock mantis shrimp
Odontodactylus scyllarus, can deliver strikes lasting only a few
milliseconds, with accelerations of over 105 m s-2 and
speeds of over 20 m s-1 (Fig.
1; Patek et al.,
2004).

One unexpected consequence of these extreme strike speeds is the generation
of cavitation at the site of impact between the mantis shrimp's heel and the
striking surface (Fig. 1;
Patek et al., 2004).
Cavitation vapor bubbles form in fluids under low pressure. This may be caused
by adjacent flow fields moving at drastically different speeds and, at their
interface, generating regions of low pressure
(Brennen, 1995;
Young, 1999). Thus, cavitation
often occurs between a solid structure's boundary layer and a rapid flow field
over its surface. Vortex cavitation commonly occurs in the vortices shed by
pumps and boat propellers, while sheet cavitation often develops in a wake or
area of separated flow and is visible along propeller blades and hydrofoils.
Cavitation generated during the mantis shrimp's strike
(Patek et al., 2004) is most
likely caused by a combination of these flow processes, including sheet
cavitation along the surfaces of the snail shell and dactyl, and the negative
pressure generated during the rapid rebound of the dactyl heel after striking
the hard surface (Fig. 1).

Peacock mantis shrimp use a pair of large raptorial appendages (A, white
arrow) to strike hard objects with such high speeds that cavitation bubbles
form between the appendage and striking surface
(Patek et al., 2004).
(B–I) The dactyl heel (h) of the raptorial appendage strikes a snail (s)
that is loosely wired to a stick. Images recorded at 0.2 msintervals. Scale
bar, 1 cm. Cavitation (yellow arrow) is visible between the dactyl heel and
snail (D–G).

When cavitation bubbles collapse, considerable energy is released in the
form of heat, luminescence and sound
(Brennen, 1995). The shock
waves and microjets generated during the collapse of the cavitation bubbles
cause stress and fatigue in adjacent surfaces, ultimately leading to failure
and flaking of surface materials (Brennen,
1995). Remarkably, a 2.7 mmcavitation bubble collapsing near a
wall can generate over 9 MPa of impact pressure over a period of approximately
5 μs (Shima et al., 1983;
Tomita et al., 1983). Such
cavitation forces can destroy rapidly rotating boat propellers, aid in
water-based metal cutters, and are even thought to provide the mechanism by
which water picks remove dental plaque
(Brennen, 1995).

The presence of cavitation is often detected acoustically because the sound
of cavitation bubbles collapsing contains greater energy at higher frequencies
than similar events without cavitation
(Brennen, 1995;
Lush and Angell, 1984;
Martin et al., 1981). Thus,
the acoustic signature of cavitation is the presence of a broadband signal
extending, with substantial energy, into the ultrasonic range (above 20 kHz),
as compared to events without cavitation that lack power in the ultrasonic
acoustic range. This phenomenon has been examined extensively in the
engineering literature, including controlled studies in which cavitation is
present and absent, as well as correlative studies linking cavitation damage
with the acoustic power of the signal in the ultrasonic range
(Brennen, 1995;
Ceccio and Brennen, 1991;
Lush and Angell, 1984;
Martin et al., 1981).
Cavitation has also been detected via acoustic analyses, especially
in the ultrasonic range, in studies of tree xylem cavitation
(Ikeda and Ohtsu, 1992;
Perks et al., 2004;
Tyree et al., 1984) and fern
sporangia (Ritman and Milburn,
1990).

The presence and dynamics of cavitation can also be detected visually.
Extreme high-speed video is necessary to capture the microsecond timescales of
cavitation bubble formation, luminescence and collapse. Cavitation bubbles in
snapping shrimp were visualized using high-speed video, coupled with the use
of a photodector to detect the emission of luminescence
(Lohse et al., 2001). The
simple presence/absence of cavitation vapor bubbles has been examined in
x-rays of joints after knuckle-cracking in humans
(Unsworth et al., 1971) and
light microscope images of fungal spores
(Money et al., 1998).

Despite our rich understanding of crushing forces and their influences on
shell evolution, as well as a substantial body of work on the physics of
cavitation, little is known about the impact forces generated by biological
hammers and biological cavitation. The mantis shrimp's unusual mechanism for
breaking shells suggests fundamental questions about the amplitude of the limb
impact forces and relative contribution of cavitation forces. Here, through
the use of force transducers, acoustic analyses and high-speed video, we
report the limb impact and cavitation forces generated by the peacock mantis
shrimp Odontodactylus scyllarus. The goals of this study were to (1)
visualize limb impact and cavitation while measuring forces, specifically to
identify the presence and relative contribution of cavitation to force
generation; (2) measure the timing and acoustic signature of impact and
cavitation; and (3) measure amplitude of forces across a range of striking
surface geometries in order to assess the effects of striking surface on the
amplitude of cavitation and impact forces. This study provides the first
in-depth examination of a biological hammer and reveals a potent combination
of power amplification, extreme impact forces and cavitation dynamics.

Materials and methods

Study animals

Thirteen peacock mantis shrimp Odontodactylus scyllarus L.
(Crustacea, Stomatopoda, Gonodactyloidea, Odontodactylidae), ranging in size
from 27 to 36 mm carapace length, were purchased from commercial collectors.
Animals were held at 25°C in recirculating artificial saltwater, and were
fed a diet of fresh snails and freeze-dried and frozen shrimp. Because of
their unpredictable molt cycles, different combinations of individuals were
used in each of the experiments. During a molt, animals were unable to strike
for several days, and only gradually recovered full striking strength. We
therefore tested animals only when they were in an intermolt period. Animals
regularly struck objects coated with shrimp paste and most animals were
willing to strike objects under bright video lights after a period of
training. In natural conditions, peacock mantis shrimp carefully position a
snail on a firm surface or anvil-like rock, and then deliver a blow that
typically causes little movement of the snail. In this study, a force sensor
(load cell) was mounted at the base of an aluminum beam that was manually
presented to the mantis shrimp. This arrangement permitted minimal movement of
the apparatus when struck.

Synchronous high-speed video and force sensor analysis of force
peaks

Cavitation processes were visualized through the use of high-speed video.
Digital video images were collected at 100 000 frames s-1 (∼0.3
mm pixel-1, 10 μs shutter speed, Ultima APX high speed camera
and Multi Channel Data Link, Photron, San Diego, CA, USA) and were
synchronized with a one-axis force sensor (force range 444.8 N, upper
frequency limit 75 kHz, Model 200B02, PCB Piezotronics, Depew, NY, USA)
sampled at 100,000 samples s-1. The kinematics of the recorded
movements were analyzed using a custom computer program (Matlab v7.0.1, The
Mathworks, Natick, MA, USA). The distance moved by the limb across each frame
was calibrated, using a structure within the image sequence with known
dimensions.

Acoustic analyses of impact and cavitation

In addition to image analysis, we measured the acoustic signatures of limb
impact and cavitation. We simultaneously measured strike forces and sound when
mantis shrimp struck curved and flat force-sensor surfaces. Sounds generated
during strikes on curved and flat surfaces were measured using a hydrophone
(1–170 kHz TC4013 hydrophone, 1 Hz–1 MHzVP2000 voltage
preamplifier; Reson Inc., Goleta, CA, USA). Acoustic data were collected at
500 000 samples s-1, using a data acquisition board
(PCI-DAS4020/12, Measurement Computing, Middleboro, MA, USA) and custom
computer data acquisition programs (Matlab v7.0.1). The onset of the first
peak was detected automatically with a threshold of 0.05 V above the average
value of a 100-sample window. The second peak onset was set at 0.05 V above
the average value of a 40-sample window following the first peak. The second
peak duration was set to the same duration as the first peak.

The power spectral density of each acoustic peak was calculated using a
multitaper method (discrete-time Fourier transform, nonparametric pmtm
periodogram, Matlab v7.0.1). The short duration of the Fourier transforms
resulted in a loss of low frequency resolution below approximately 2 kHz. The
maximum amplitude of the acoustic data was scaled to 1 V prior to comparing
the power spectral density across events. For the flat surface tests, acoustic
data were collected for five individuals (3–5 strikes per individual).
For the curved surface tests, acoustic data were collected from six
individuals (4–21 strikes per individual).

One-axis analysis of impact and cavitation forces

We used a one-axis force sensor to measure the relative contributions of
limb impact force and cavitation force (force range 444.8 N, upper frequency
limit 75 kHz, Model 200B02, PCB Piezotronics, NY, USA). The stainless steel
force sensor had a 12.7 mm diameter load surface and a stiffness of 1.9 kNμ
m-1. Data were collected at 500,000 samples s-1
using a data acquisition board (NIDAQ 6062E, National Instruments, Austin, TX,
USA). Peak forces (amplitude of force trace) and force impulse (integrated
area under a force curve; Caldwell et al.,
2004; Ozkaya and Nordin,
1999) were analyzed using custom-designed computer analysis tools
(Matlab v7.0.1). The onset of the first peak was set as an increase of 0.05 V
above the average value of a 100-sample window. The second peak onset was set
at 0.08 V above a 40-sample average window after the first peak. The ends of
the first and second peaks were set to the same value as the onset voltage for
each peak.

Video recordings (60 frames s-1, Sony DCR-VX2100, Sony Corp.,
New York, NY, USA) were simultaneously collected in order to establish whether
the force sensor was struck by one or both raptorial appendages. Both peaks
were analyzed if only one raptorial appendage struck the force sensor. If two
raptorial appendages struck the force sensor in close succession, four force
peaks were logged, leading to potential ambiguity as to the source of each of
the four peaks. In these cases, only the first peak was included in the
analysis. Some individuals exceeded the capacity of the load cell, thus any
force data that exceeded the linear range of the load cell (>445 N)
wereremoved. After the overloaded data had been removed, the final dataset
reported here included four individuals with 6, 12, 22 and 25 strikes per
individual.

Three-axis force analyses of strikes on curved and flat surfaces

We measured the effects of surface geometry on force generation through the
use of curved and flat surfaces. For the curved sensor, we measured the radius
of curvature of a range of snails typically consumed by these mantis shrimp
and machined a curved cap for the force sensor with the average measured
radius of curvature (9.7 mm curvature; 28.5 mmsolid, 300-series stainless
steel from strike surface to sensor surface). The flat sensor was 24.1
mm×24.1 mm, with 18.1 mm solid, 300-series stainless steel from strike
surface to sensor surface.

Strike forces on curved and flat surfaces were compared using a waterproof,
three-axis, piezoelectronic force sensor designed for measuring impact forces
(force range 1334 N in each axis, 90 kHz upper frequency limit, <4.1%
cross-talk between axes; W20M25/010G10, PCB Piezotronics). The z-axis
was designated as a horizontal force `into' the sensor. The y-axis
was defined as a vertical force, and the x-axis represented lateral
forces.

The peak amplitude of forces in the three axes was measured using a custom,
automated computer program and forces from each axis were summed using
standard vector calculations (Matlab v7.0.1). The onset threshold of the first
force peak was set as 0.02 V above the average value of a 100-sample window;
the onset of the second force peak was set as 0.05 V over a 40-sample average
window following the first peak.

The thick and heavy steel caps on the three-axis force sensor generated
long reverberations, which prevented unambiguous quantitative measurements of
impulse at less than 1 ms after the initial impact. Thus, although we could
measure the amplitude and the relative timing of the multiple peaks, it was
not possible to report conclusive impulse data after the initial force peak.
Some animals exceeded the capacity of this force sensor and these data were
removed from the analyses. With these data removed, our final dataset
included, for the flat sensor tests, ten individuals (5–20 strikes per
individual) and for the curved sensor tests, six individuals (4–23
strikes per individual). Video recordings (60 frames s-1; Sony
DCR-VX2100, Sony Corp.) were simultaneously collected in order to establish
whether the force sensor was struck by one or both raptorial appendages.

Statistical analyses

Values are means ± s.d. One-way analysis of variance
(ANOVA) was used to assess individual variation in the temporal aspects of
force generation. The scaling of force with carapace length and dactyl heel
width was evaluated with a linear regression. Statistical software was used
for these calculations (JMP 5.0.1, SAS Institute, Inc., Cary, NC, USA).

Results

Synchronous high-speed video and force sensor analysis of force
peaks

Cavitation vapor bubble formation, collapse and rebound were visible with
ultra-high speed imaging. We analyzed the temporal correlation between force
generation, limb impact and cavitation bubble collapse using the video and
force data. A single strike by a single appendage generated two force peaks in
rapid succession (Figs 2,
3). The individual mantis
shrimp used in this study only had one raptorial appendage, thus allowing us
to rule out fast double-strikes as the cause of the two force peaks. In all
strike sequences, the first force peak corresponded with limb impact and the
second force peak occurred during cavitation bubble collapse (Figs
2,
3). Videos are available online
as
supplementary material.

Acoustic analyses of impact and cavitation

Consistent with the video analysis above, each strike generated two peaks
in both the force data and acoustic data, regardless of whether the striking
surface was curved or flat (Fig.
4). Spectral power analysis showed that second acoustic peaks
typically contained more energy at higher frequencies (above 40 kHz) than
first peaks in both curved and flat surface experiments
(Fig. 5,
Table 1). The times between the
first and second acoustic peaks were 390±54 μs on the curved surface
and 472±49 μs on the flat surface
(Table 2).

Limb movement and force generation. The heel of the raptorial appendage
(purple, right y axis) approaches the force sensor (located at
distance 0, right y axis) and generates force (black, left y
axis) during impact (peak 1) and when cavitation bubbles collapse (peak 2).
Negative pressure as the limb rebounds from the sensor surface is indicated by
the slight negative excursion of the force trace between the first and second
force peaks. Distance data was digitized from high-speed video (100,000 frames
s-1) and smoothed using the negative exponential function
(polynomial regression and Gaussian density function; SigmaPlot v.9.0,
Systat). The one-axis force sensor was sampled simultaneously at 100,000
samples s-1.

One axis analysis of impact and cavitation forces

We used a one-axis force sensor to measure the relative contribution of
limb impact force and cavitation force, both in terms of peak force and
impulse (Fig. 6). We found that
the cavitation forces were an average of 50% of the limb impact forces, and
reached a maximum of 280% of the limb impact force within a given strike
(Table 3). The ratio of the
second peak to the first peak force was not significantly different across
individuals in the peak force, but the ratio of the second impulse to the
first impulse did vary significantly across individuals (one-way ANOVA; peak
force: P=0.8486; impulse: P=0.0004). The average time
between the first and second peak was 410±60 μs
(Table 2), with significant
differences across individuals (one-way ANOVA, P<0.0001). The
duration of the first peak averaged 49±18 μs and the second peak
averaged 66±28 μs.

The formation, collapse and rebound of a cavitation bubble between a mantis
shrimp's dactyl heel and a force sensor. The left trace (blue) indicates force
output from a force sensor that was recorded synchronously with high-speed
images at 100,000 samples s-1. The series of photographs on the
right are recorded at 0.1 ms intervals (from the top down) and temporally
aligned with the horizontal lines in the force trace. The two images on the
left correspond with the two maximal force peaks. The formation of a
cavitation bubble begins when the limb strikes the force sensor (1). The
cavitation bubble collapses at the onset of the second peak (2), and then
rebounds (3) until the last shown image. This sequence of cavitation bubble
formation, collapse and rebound is typical of cavitation occurring near a
boundary, in which peak force occurs during cavitation bubble collapse
(Brennen, 1995;
Tomita and Shima, 1990).
Termed the rebound phase, a small cloud of bubbles is typically formed after
the initial collapse of the primary cavitation bubble. These smaller bubbles
will continue to collapse, but with smaller resultant forces than the collapse
of the first large cavitation bubble
(Brennen, 1995;
Tomita and Shima, 1990).
Videos of simultaneous force and video traces are available online as
supplementary material.

Three-axis force analyses of strikes on curved and flat surfaces

The three-axis force sensor showed that cavitation forces were typically
half the amplitude of the limb impact forces, although in some strikes, the
cavitation forces reached 140% of the limb impact forces
(Table 4). The average time
between impact and cavitation was 390±54 μs for the curved surface
and 480±71 μs for the flat surface
(Table 2). The ratio of the
second peak force to the first peak force was not consistently significantly
different across individuals (one-way ANOVA; curved cap, P=0.7264;
flat cap, P=0.0009). Time between the first and second force peak was
significantly different across individuals (one-way ANOVA; curved cap,
P <0.0001; flat cap, P=0.0015).

Limb impact generated an average 472 N peak force summed across the three
axes on the curved surface and 693 N on the flat surface, with maximum
recorded forces reaching 983 N and 1501 N, respectively
(Table 4). For the curved
surface, animals generated peak forces of 1118–1917 times their body
weight. With the flat surface, individuals generated peak forces of
1420–2624 times their body weight.

Typical strike force (A) and sound (B) of a single limb striking a
three-axis force sensor (only the z-axis data are shown here). Note
that there is a slight offset in timing between the force and acoustic data;
this offset is due to the approximately 62 μs necessary for the sound waves
to reach the hydrophone, which was located several cm from the force
sensor.

Comparison of relative power spectra between the first (blue) and second
(green) acoustic peaks recorded as mantis shrimp struck a three-axis force
sensor. The curved surface (A) and flat surface (B) yielded similar spectral
distributions. Second peaks (green) typically contained more energy at higher
frequencies in the ultrasonic range (above 20 kHz) than first peaks, which is
consistent with cavitation being the source of the second peak
(Brennen, 1995;
Lush and Angell, 1984;
Martin et al., 1981). The peak
amplitudes of the acoustic recordings were scaled to 1.0 prior to conducting
Fast Fourier Transforms, thereby allowing comparisons of relative
power/frequency of first and second peaks within a given strike and across
strikes.

The majority of the force was delivered through the z-axis with
similar force profiles for both flat and curved sensors (flat: z,
77±7%; y, 12±5%; x, 11±6%; curved:
z, 79±7%; y, 12±5%; x, 9±7%;
all values mean ± s.d.).

Force generated when a mantis shrimp strikes with both raptorial
appendages. Four force peaks are detected by a one-axis force sensor when
struck by two raptorial appendages. Based on the high-speed video and acoustic
analyses above, the two higher peak forces were generated by limb impact and
the two lower peaks were generated during cavitation bubble collapse.

Discussion

Shell-breaking forces have historically been analyzed in terms of two
predator strategies: crushing (repeated compression of whole shell until
failure) and peeling (chipping away the lip of a shell until soft tissue is
exposed). A single pulse of compressive crushing force, sufficient to break
sturdy molluscan shells, ranges from hundreds to thousands of Newtons applied
over a period of seconds (Vermeij,
1987; Vermeij and Currey,
1980). On the other hand, effective peeling requires a fraction of
these crushing forces (Preston et al.,
1996). Studies of the maximum force generated by crushing and
peeling mechanisms suggest that predators are constrained to breaking shells
below a certain size, or that predators repeatedly apply forces that gradually
cause cumulative fractures in the shells
(Preston et al., 1996).
Indeed, predators most typically apply crushing forces multiple times for each
shell, with each force application lasting for periods of hundreds of
milliseconds up to multiple seconds (e.g.
Kaiser et al., 1990;
Korff and Wainwright, 2004;
Zipser and Vermeij, 1978).

In contrast to crushing and peeling mechanisms, the mantis shrimp's hammer
generates forces ranging from hundreds to over a thousand Newtons, delivered
over microsecond timescales (Tables
3,
4). A strike with a single
appendage generates two force peaks, approximately 0.5 ms apart, with the
first force peak caused by limb impact and the second peak generated by
cavitation bubble collapse (Figs
2,
3,
4). A strike with both
appendages, therefore, generates four force peaks in extremely rapid
succession (Fig. 6), at time
scales on the order of 1000 times shorter than typical, cyclically applied,
crushing forces.

While the absolute values of these peak forces are well within the range of
crushing forces, mantis shrimp generate forces that are thousands of times
their body weight, exceeding, by far, previous estimates of maximum force
production (on the order of hundreds of times body weight)
(Alexander, 1985;
Taylor, 2000). Thus, the
hammering mechanism allows mantis shrimp to generate peak forces that far
surpass the peak forces generated by shell-crushers of similar body size.
However, these high force peaks are delivered over very short time periods,
typically 49 μs and 66 μs, for the impact and cavitation forces,
respectively. As a result, the impulses of the strikes are typically on the
order of a fraction of a μNs.

Inelastic impacts on hard substrates cause a rapid change in acceleration
over a very short time period and thereby generate high peak forces and low
impulses. The material properties of a substrate can influence the recorded
peak forces, through the time course of this change in acceleration and
associated absorption of energy. Thus, the peak forces produced by mantis
shrimp in this study should be interpreted in the context of the steel
surfaces that they struck; a more energetically absorptive surface would yield
lower peak amplitudes. However, the presence of cavitation appeared not to be
influenced by the material properties of the striking surface; cavitation was
consistently observed in naturalistic strikes of force sensors and snail
shells (e.g. Figs 1,
3) and even when animals struck
rubber corks (R.L.C. and S.N.P., personal observation). It is worth noting
that the particular strategy employed by mantis shrimp, that of using
sequential applications of brief high magnitude forces, is well known to
engineers as an effective mechanism for fracturing composite materials,
specifically via rapid jets and ballistic impacts
(Meyers, 1994).

Perhaps even more surprising than the high peak forces is the observation
that mantis shrimp couple these impact forces with the implosive force of
cavitation bubble collapse. While on average the cavitation forces were half
those of the impact forces, in many cases the cavitation force actually
exceeded those of the limb's impact (Tables
3,
4). In both the thin-surface,
one-axis force sensor and the thick, solid steel, three-axis force sensors,
cavitation forces played a substantial role in force generation, suggesting
that this phenomenon is robust across surface geometries, surface thickness
and mass (Tables 2,
3,
4). The combination of impact
fractures and the surface stresses caused by cavitation may be effective for
damaging the composite, ceramic layers of a mollusk shell
(Vincent, 1990). In future
studies, it would be informative to mount strain gauge force transducers to
actual shells and to examine the relative damage imposed by limb impact and
cavitation forces, especially in relation to the material properties of a
shell. Indeed, to our knowledge, experimental tests of shell fracture
mechanics in response to hammering with an appendage have not been previously
studied.

Acoustic analyses of mantis shrimp strikes also yielded information about
the presence of cavitation. The majority of the acoustic power was contained
in the collapse of the cavitation bubble, with the acoustic power of the
cavitation bubble collapse averaging 1.2–1.6 times the acoustic power of
the limb impact (Table 1). The
spectral distribution of the two sound peaks differed primarily in the
ultrasonic range (Fig. 5),
thereby supporting the hypothesis that the second acoustic peak was generated
by cavitation bubble collapse, which is characterized by a broadband acoustic
signature with substantial energy into the ultrasonic range
(Brennen, 1995;
Lush and Angell, 1984;
Martin et al., 1981).
Ultrasonic acoustic measurements of mantis shrimp strikes may be helpful in
future studies for establishing the presence and absence of cavitation under
different depth conditions or when smashing particular substrates,
specifically through identification of two acoustic peaks and the presence of
a broadband ultrasonic signature in the second peak.

The role of cavitation and control of cavitation by biological systems
remains an interesting and wide-open area of biological research, and perhaps
it is time to consider the evolutionary history of cavitation, even if only as
an epiphenomenon. Cavitation phenomena are sensitive to ambient pressure and
impurities in the water, such that cavitation bubbles form more readily at low
pressures and in aerated and impure water (such as saltwater). Thus, it would
be interesting to incorporate depth as a factor in evolutionary analyses of
biological cavitation structures, because organisms at depths of greater than
100 m are far less likely to induce cavitation
(Smith, 1996).

The subject of this study, O. scyllarus, is a shallow water
species and is typically found to a depth of 3–30 m
(Ahyong, 2001;
Manning, 1967). However, the
genus Odontodactylus includes some of the deepest living smasher
stomatopods. While most odontodactylids are found living shallower than 50 m,
O. hawaiiensis occurs to depths of greater than 100 m
(Manning, 1967;
Retamal, 2002) and O.
brevirostris has been reported to depths of over 400 m, although
generally this species is found in the 15–40 m range
(Manning, 1967). Most other
Gonodactyloidea smashers are found at less than 40 m, although several occur
to 80–100 m and Echinosquilla guerini is found to 200 m
(Ahyong, 2001). Some of the
deepest small gonodactylids seem to have changed their predatory behavior and
concentrate on small prey taken in the water column or prey that does not
require heavy smashing (R.L.C., personal observation). There are, of course,
multiple explanations for these depth distribution patterns. For example,
mineralization is more difficult in colder deep water, such that mollusks and
crustaceans are not as well-mineralized
(Vermeij, 1987) and powerful
hammers may be neither necessary nor possible.

The inherent challenges in the design of a failure-resistant, biological
hammer may explain why, outside of stomatopods, relatively few species hammer
shells (Currey, 1967;
Vermeij, 1987). It is
intriguing that mantis shrimp do not fracture their own exoskeleton during
these strikes. Mantis shrimp raptorial appendages show wear over time and they
molt regularly to grow a new exoskeleton. Nonetheless, in between molts,
smasher mantis shrimp generate tens of thousands of blows
(Caldwell et al., 1989;
Full et al., 1989) with a
destructive combination of high impacts and implosive cavitation events. In
addition to shell hammering, many stomatopods also strike rocks, coral and
coralline algae for den construction. This raises fundamental questions as to
the mechanical and material properties of the dactyl heel, about which we know
little.

Currey et al. (1982)
examined the raptorial appendages of an alcohol-preserved
Gonodactylus specimen and found that the outer layer of the dactyl
heel is highly calcified and covers a layer of fibrous cuticle, within which
soft tissue is located. Microhardness tests yielded higher values along the
outermost cuticular layer, as compared to the inner fibrous layer.
Interestingly, microhardness correlated positively with the ratio of
phosphorus to calcium in the heel's surface. Currey et al.
(1982) also noted that the
outermost layer was highly brittle, but that cracks did not propagate into the
fibrous layer. Further studies of material and mechanical properties of the
mantis shrimp's limb may hold clues for engineered materials that are
resistant to both cavitation and impact forces.

It is not presently known how and whether shells respond differently to
crushing forces, impact forces and cavitation forces. Mantis shrimp evolved a
ballistic raptorial appendage during the Carboniferous
(Schöllmann, 2004, F.
Schram, personal communication), and a true smashing appendage at least by the
Eocene, in what appears to be an odotondactylid (C. Hof, personal
communication). It is possible that this unusual method of breaking snails has
played an important, but currently unexamined, role in the evolution of shell
form in stomatopod prey populations. Mantis shrimp provide a remarkable
example of biological cavitation coupled with high impact forces which, in
combination, appear to be tremendously effective in fracturing shells.

Schöllmann, L. (2004). Archaeostomatopodea
(Malacostraca, Hoplocarida) from the Namurian B (Upper Marsdenian,
Carboniferous) of Hagen-Vorhalle (NRW, Germany) and a redescription of some
species of the family Tyrannophontidae. Geologie und
Paläontologie in Westfalen62,111
-141.